Sensory Functions: Proceedings of the 28th International Congress of Physiological Sciences, Budapest, 1980

Sciences

SOMATO-SENSORY THALAMIC UNIT ACTIVITIES RECORDED IN CHRONIC AWAKE ANIMALS. MODIFICATIONS PROVOKED BY PERIPHERAL AFFERENT DEPRIVATION AND CENTRAL INHIBITORY INFLUENCES

D. Albe-Fessard, B. Hamon, P. Cesaro and B. Pollin,     Laboratoire de Physiologie des Centres Nerveux, Université Pierre et Marie Curie 4, place Jussieu, 75230 Paris, France

Publisher Summary

The connexions and the organization of somato-sensory thalamic centers were first studied in animals under general anesthesia. However, the opposite changes obtained in evoked cell responses when different classes of anesthetic were used has caused misunderstanding between groups of physiologists, each group having the impression that the mode of anesthesia they used was the most similar to natural sleep. To have a better image of normal thalamic activities, awake animals had to be utilized. They were very awake when implanted with macro-electrodes or awake and curarised with local analgesia of the fixation points when microelectrodes were used. In a group of 7 macaca cynomolgus having received a spinal cord lesion, the thalamic organization of the thalamus was studied. This lesion suppressed the dorsal columns and Morin’s bundle on one side at the T5 level. These partial lesions have been found to produce a change in thalamic organization.

The connexions and the organization of somato-sensory thalamic centers were first studied in animals under general anesthesia. However, the opposite changes obtained in evoked cell responses when different classes of anesthesic were used has caused misunderstanding between groups of physiologists, each group having the impression that the mode of anesthesia they used was the most similar to natural sleep. To have a better image of normal thalamic activities, awake animals had to be utilized. They were totally awake when implanted with macroelectrodes, or awake and curarised with local analgesia of the fixation points when microelectrodes were used. It is not sure however that in this latter case pain is totally avoided, moreover it is not certain that curarising agent and local analgesic have no central effects at all. Furthermore, when the animals are curarised, for comparable results the composition of the expire air has to be measured, a condition easy to fulfil in Monkeys and Cats, but difficult in Rats. For all these reasons, we have developed techniques allowing chronic recordings in the three just-quoted species. They permit the use of classic stereotaxic techniques and glass micropipettes. Yokota and Mac Lean (36), Woody and different collaborators (30, 31, 33) were the first to use similar techniques which were more recently used also by Richard et al. (28), our group (2,6,26) Rougeul et al. (30). For Monkey and Cat, our technique is modified from the one used by Yokota and Mac Lean (36). For Rats, due to the space limitation, the technique of Noda et al. (25) was prefered (see Sapienza et al. 33).

In all the three cases the head was fixed during the recording. It was linked, by a device screwed in the bone, to the bars of a stereotaxic apparatus so that the head was in a stereotaxic position. The animal’s body was otherwise free. It was seated in a chair (Monkey), lying on the table (Cat) or in a hammock (Rat) in such a way that peripheral fields were easy to examine. The bone was removed (the dura-mater being respected) at the level where microelectrodes would be introduced afterwards, and replaced by a plastic box, filled daily with surgicel and tifomycine. The glass microelectrodes were introduced through the dura mater. The stereotaxic coordinates were taken from the Atlas of Kusuma and Mabuchi (). We have systematically utilised glass micropipettes and no filter in the recording line, so as to be able to recognise through their shape, spikes recorded from soma or axon. Figure 1 gives an example of different spikes recorded at same sweep speed. The shape of a soma spike can vary from monophasic negative or positive to diphasic whereas the axon spikes are always monophasic positive. The duration of spikes are also different. Those two characteristics allowed to recognised axon and soma even when they are intermingled, as it happens in nuclei (4).

Figure 1 Chronic Cat – Recordings with glass micropipette of two different axons and three different cell-bodies at thalamic level. For this figure and the 7, 8 and 10, negativity is upward.

Mapping of the somatic thalamus was performed for the three species. We will only report here the main characteristics of the awake cat thalamic map and utilise those characteristic to understand the effect of deafferentation and the role of an inhibitory system.

I THALAMIC ACTIVITIES AFTER PARTIAL AFFERENT DEPRIVATION

In a group of 7 macaca cynomolgus having received a spinal cord lesion, the thalamic organization of the thalamus was studied (26). This lesion suppressed the dorsal columns and Morin’s bundle on one side at the T5 level. These partial lesions have been found to produce a change in thalamic organisation. When the VP of lesioned macaca was compared to the VP of normal macaca, we observed that the representation of the leg whose afferents were suppressed was replaced by the representation of the arm (see 26 and figure 2). Those results could be explained in two different ways : – The spinal lesion we had performed allowed the disclosure of a preexisting projection, – Sprouting of non-lesioned afferents appeared at the thalamic level or in a previous relay.

Figure 2 Chronic Monkey – Representation at same anterior plane of the localisations of cells driven by arm and leg, in normal monkeys (at left) and in monkeys having received a section of dorsal column bilaterally and of Morin’s bundle in the right side at the T3-T5 level (schema in the lower right corner). (slightly modified from 25)

Those hypotheses have also been advanced by others to explain similar results obtained at spinal cord level in the Cat (23) and bulbar and thalamic level in the Rat (24, 34). No decisive experiments have been performed until now, which permit a choice between those two explanations, and experiments done in animals with different times of survival have still to be performed. However the need to have a large number of observations drove us to employ cats and rats before returning to macaca.

Thalamic maps in normal Cats

Our main problem when working in Monkey was to have a reference map of the awake Monkey thalamus (12), thus our first goal was to reexamine the thalamus of awake Cats and Rats not undergoing the stress of painful restraint. Recordings were frequently made at cortical level in chronic monkeys and cats with metallic microelectrodes, on the contrary similar observations are scarce in thalamus of cats (2, 5) and absent in Rats. In Cats the existing map is only partial and a new systematic mapping was necessary.

The technique of glass electrode recording in chronic animals has its difficulties. The main one is a good localisation of the recorded units. The system of head fixation adds an appreciable source of error to the normal stereotaxic variation and good histological localisation is necessary. For this purpose, the micropipettes were filled with KC1 0,75 M to which pontamine blue was added. They were driven into brain tissues using a calibrated microdrive and at the terminal point of the track the dye was ejected by iontophoresis. The localisation of the dyed point can be seen after a survival time of one month. The number of microelectrode tracks had to be low (7 to 8 per thalamus) to obtain good identification of the tracks. In brief for all these reasons we were not able to use for mapping all the explorations we have performed and the maps we are presenting are based on the recordings obtained in three cats and only on the thalamic trajectories that were clearly recognised (24 trajectories).

Among 810 units studied at thalamic level we recognized 740 spikes from somata and 70 from axons. Among the soma units we separated afterwards those that had a contralateral localised peripheral field from those with a large, frequently bilateral, field. Figure 3 gives an example of this classification in 4 stereotaxic planes. Similar observations were done from plane Ant. 5 to plane Ant. 11. It is interesting to note that cells with localised peripheral fields appear in VP but also in LP. At these different levels the cells were afterwards classified for their type of optimal receptor and their peripheral field position on the body surface. We called tactile units those cells responding to movement of hairs or light stroking of glabrous tissues ; joint units : those activated by claws and more proximal articulations of the limbs ; movement units, those activated by movements and pressure on muscles. The other units were driven by light taps on superficial or deep tissues. Finally some units were only driven when relatively strong stimuli were used (pinching, strong taps, etc.). We called them nociceptives. We have to note that intense nociceptive stimuli which disturb the cat strongly were never used in our chronic preparation. These different types of units appeared in all the thalamic areas. But tactile and joint units were the most frequent in VP (a few were however in LP) nociceptives units were in posterior regions (a majority in LP, MG mc, n. Reticularis), movement units were more anterior. Somatotopy existed only in VP and was not exactly the medio lateral disposition classically described (figure 4). Head and anterior limb representation were essentially present in the planes 7.5, 8.5 and 9.5 and the posterior limb representation appeared only in the more anterior planes, small at 9.5, important at 10.5 level. At 10.5 level, head representation was practically absent. These results are in a good agreement with those obtained anatomically by Rinvik (29).

Figure 3 Chronic Cat – Composite thalamic maps at 4 frontal levels of results from explorations in 3 chronic cats. White circles represent fibers all the dark symbols correspond to cells. Cells without peripheral field horizontal bars. At Ant. 10.5 stippled area is a zone where a total silence was found.

Figure 4 Somatotopy in chronic Cat : Same results as for figure 3. But here only cells having a relatively restricted peripheral field were plotted. For the peripheral field localisation, see the figurine : triangles correspond to pressure on the belly or the viscera.

The common type of convergence on a cell of afferents coming from different area was found in many regions (LP, MD, Ret.). But a more interesting convergence was the one in which same cell was activated by two localized peripheral stimuli. We found 11 of these cells in VP. They were activated by two separate localised tactile stimuli (2 cells) (discontinuous field on the face and on the anterior extremity), cells with tactile localised field and pinching, or tapping or muscle pressure in another zone (9 cells). Tactile field and visual excitation or inhibition appeared also. Similar observations were made in Monkeys where a constant light stimulus made a tactile response appear. The convergence on the same cell of different messages coming from localised areas was frequent in zones of transition for example that between face and hand representations or at the place where VP is proximal to GL. With these convergences we had a basis for explaining the appearance of new representation if it revealed itself in Cats. However, the small number of VP cells having this property can explain the phenomenon only if it is a small one, even if the number of cells with convergence we have observed is certainly a low estimate. More convergence will probably be demonstrated when implanted stimulation is used. In monkeys, in which this type of experiment has been done, we have shown that different types of fibers having different speed can converge on the same cells.

Thalamic maps in Cats with partial afferent deprivation

We used the technique just described to study the thalamus of cats in which a number of dorsal roots have been sectioned. Different extents of lesion have been used, but we are reporting here the results obtained in a Cat in which five roots were sectioned between dorsal ganglia and spinal cord at C5, C6, C7, C8, T1 level, section which corresponds to a maximal denervation of the extremity of the anterior limb (13). The animal recovered well from the operation and the surgical field healed rapidly. A month later a wound due to strong repetitive scratching appeared at the arm level on the side of the root lesions. These wounds increased in area during the following month and were still present but on the way to healing when the recordings were performed 6 months after the root sections. This animal presented the same defect due to scratching that was described in the Rat after similar root lesions by Lombard et al, (20) (Cats never performed the automutilations seen in Rats), When the maps of the thalamus contralateral to the dorsal root lesions were made, little change could be seen in the number of cells having peripheral fields. We found for example in plane 9.5, 46 cells activated among the 129 units encountered compared with 68 cells among 131 units in the same region of normal cats. Differences began to be seen only when somatotopy was studied. These changes were evident at VP level only. We present here the results observed in plane Ant. 9.5 (figure 5A) and compare them to those obtained in normal cat. It can be seen that in a region where arm representation is normally present leg and face representation have taken its place. The modification is even clearer if the projection from maximally disconnected limb is considered as in figure 5B, It can be seen that elbow and arm representations increase and partly replace, together with leg and face, the hand and forearm. Moreover tactile representation of the arm has mostly disappeared and been replaced by deep afferents activated by pressure and pinching of arm and elbow. As we have said, this change could be due to a previous convergence of the new peripheral field on the thalamic cell. But sprouting effects cannot totally be discounted, and new experiments with different times of survival as well as anatomical observation to see if new connections are present have to be performed before a final conclusion be given to this type of experiment.

Figure 5 Composite figure showing the change observed in the Cat thalamus map when dorsal roots C5 to T1 were sectioned. A – In plane 9.5, the somatotopic organisation is presented in intact animal (at left) and in animal having received root sections (at right). B – Two trajectories made at same stereotaxic level are compared in an intact and an operated cat. Note that afferents from forearm and hand are replaced by arm, elbow, leg and head afferents.

II SPONTANEOUS CELL FREQUENCIES IN THALAMIC AREAS OF CHRONIC ANIMALS

Recording in the brain of 15 cats and 9 rats, we were always impressed by the large thalamic zones that were totally or almost silent. The spontaneous level of firing in a quiet chronic animal is more similar to what is observed in a deeply anesthetized preparation (chloralose or nembutal) than what is observed in an awake but curarised animal having a controlled gaz exchange. The major spontaneously active region is in and just around ventralis posterior. Two different areas of silence can be distinguished:

1°) At the antero-medial part of VP in a region still named VP by Jasper and Ajmone-Marsan (15) but not by Rinvik (29) a zone where no cell can be activated or recorded was observed (see figure 3, Ant. 10.5). To speculate, since this is a region where in normal man stimulation provokes pain (11) we can propose that the afferents arriving at this level are nociceptive but inhibited in normal animals. In favor of this hypothesis is the fact that we have found at the inferior limit of this area a dental pulp projection (2). Those propositions have however to be confirmed.

2°) In the lateralis posterior, the n. Reticularis, the Centralis Lateralis and the anterior part of CM-Pf, exist large zones where cells are only recognized by membrane noise and a few spikes of injury before disappearing. For those cells the peripheral fields are difficult to determine but some, in particular at CL-CM level, respond when a shock is applied to an implanted nerve (see figure 9), We have systematically measured the cell discharge frequencies in chronic Cats and Rats in this zone. An example is given of a frequency map obtained at the medial thalamic level in Rats (figure 6), We can note here the large number of cells having a frequency under 2 per second.

Figure 6 Chronic Rat – Frequencies (in hertz) of the spontaneous discharges recorded in 3 Rats at two different medial thalamic levels.

Figure 9 Two examples of the effect of striatal stimulation recorded on chronic animals. A– Chronic Cat : a cell in NCP presented a short latency response to the stimulation of radial nerve implanted with chronic electrodes. A repetitive stimulation of the caudate (10 shocks at 100/sec) suppressed this response and the spontaneous activity when applied before the radial nerve stimulation. When the current intensity of the caudate stimulation was progressively reduced the response to radial nerve reappeared. The raster-display must be read from bottom to top. B- Chronic Rat : one shock applied at striatum level produces first a short latency response and afterwards an inhibition followed by rhythmic bursts. Responses of same cell is presented twice as well as the corresponding raster-display.

A fraction of these relatively silent cells showed slow bursting (figure 7). These bursts are present only in some cells of the silent thalamic areas (see also 14). In 3 chronic cats, we determined the zone where they appeared (figure 7A). They were found in majority in the Reticularis Thalami, and the dorsal LP and CL. In other planes, they appeared in CL and CM-Pf. These bursts present in the awake but quiet animal can disappear when an alerting stimulus is applied (click, light, pinching, etc‥). Frequently not all of those stimuli are effective and one of them is the most powerful. Certain of these units have a large somatic peripheral field. Two examples are given in figure 7B of cells bursting in LP. In one of these cells, the burst of spike appears on a large positive wave which does not appear when a stimulus has activated the cell. This fact implies that during the bursting phase the cell is hyperpolarised. Those observations are all in favour of the action at thalamic level in awake but quiet animals of an inhibition acting on a large thalamic zone, and responsible for the silence and the bursting we observed. This inhibitory control can act at different levels. The thalamic silence can be the result of an afferent suppression due to inhibition acting on previous relays (Spinal cord, Reticular formation, etc‥) or to a direct thalamic action. Considering this last possibility we have examined the different regions from which an inhibitory action can be exerted at thalamic level. Stimulation of cortical zones (1) Raphe nuclei (6) striatal (16, 17, 18) and hippocampal (21, 23) areas, have all produced inhibition in thalamic cells. We will consider today only the possible role in chronic animals of thalamic inhibition of striatal origin.

Figure 7 Chronic Cat : A– Localisation of a part of the cells presenting burst activities observed in 3 cats. B– Examples of 2 bursting cells with low frequencies (circles in A). Cells were bursting when the animal was awake but quiet (at left). The burst disappeared when a stimulus was applied (at right) (movement of limbs and pressure on limb muscles respectively). Arrows designate bursts of a third proximal cell.

Striatal influence in chronic and acute animals

The inhibitory influence exerted by the head of the caudate nucleus on medial thalamic cells was demonstrated 15 years ago by using evoked slow waves, Krauthamer and Albe-Fessard (16). This inhibition was afterwards studied at unitary level (8, 17, 21, 22, 9) in acute cats anesthetised with chloralose or encéphale isolé. The same inhibitory effect was not systematically searched for in acute paralysed animals. We have undertaken a new experimental series using curarised Rats and verified afterwards that the same results could be obtained in chronic cats and rats (figure 8).

Figure 8 Comparison of the localisation of cells the activity of which was modified by striate stimulation in acute and chronic rats (dark symbols). The cells which were not influenced are signalled by a bar. Cells were inhibited only (circles) or had also a short latency response antidromic and/or orthodromic.

A long, lasting inhibition can be produced when one shock or a short train of shocks is applied through concentric bipolar electrodes implanted in the head of the caudate or the putamen, figure 9 present examples of this sort of inhibition observed in chronic Cat and Rat and studied using raster-display. Both spontaneous activity and evoked activities due to nerve stimulation are suppressed. At medial thalamic level 50 % only of the cells demonstrate this inhibition. As can be seen in figure 8, the distribution of inhibited cells is larger in acute than in chronic animals. But it is understandable when we think that at this level the majority of cells are silent or nearly so, which render the demonstration of inhibition difficult. In fact it is for this reason that in the cat thalamus, we have studied mostly the inhibition of evoked activities. Frequently the inhibition is followed by a change in organisation of the activity, the cell becoming rhythmically active as is shown in figures 9 and 10. This effect appears equally well in Rat as in Cat.

Figure 10 A - Acute Rat - two superior rows : responses to a striatal stimulation of a cell recorded intracellularly (membrane potential of 30 mV). An hyperpolarisation (10 mV maximum) appeared during the inhibitory phase. - inferior row : same response is presented extracellularly and as a raster-display.

B - Rat - A medial thalamus cell presents both an antidromic and an orthodromic response (arrow) after a stimulus applied to the caudate. The antidromic response when produced sufficiently early after an orthodromic spike is suppressed through collision (triangle). The spontaneous spikes started the sweep.

When intracellular recordings were performed the inhibition was always accompanied by an hyperpolarisation (figure 10). As can be seen in Figures 8, 9 and 10, stimulation of Caudate does not provoke only inhibition ; 30 % of the inhibited units are also excited at short latency, and 10 % of them presented an antidromic activation whose nature was recognised by collision test.

In conclusion, a tonic inhibition from caudate origin can explain at least in part the long phase of hyperpolarisation that seems to silence medial thalamic cells. But is this inhibition truly from caudate origin, or is the stimulation we are using activating another system? The action of caudate stimulation can be explained using the three schemata of figure 11. Cells from the medial thalamus project to the caudate : this fact is well known and the appearance in our recordings of antidromic spikes is a confirmation of it (see also 18).

Figure 11 Schemata of the connections between striatum and medial thalamus which can explain the effects of Caudate stimulation (see text).

On the contrary a direct pathway from Caudate to medial thalamus has not been demonstrated and the attempt we have made to record antidromic spikes in caudate when stimulating medial thalamus has been a failure. Hence schema A is highly improbable. In consequence we have to advance two hypothesis:

– either a relay (whose locus we are still seeking) exists in an orthodromic pathway linking Caudate or fibres going through caudate and medial thalamus (schema B).

– or the inhibitory effect is due to the antidromic activation of a collateral of the medial thalamus-Caudate pathway (as was suggested by Kunze et al. (18), and presented in schema C. If this last hypothesis turns out be true, the inhibition will have its origin in the medial thalamus itself and be distributed to a large population of dorsal and medial neurons (27).

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DIVERSIFICATION AND SYNTHESIS OF SENSORY SYSTEMS ACROSS THE CORTICAL LINK

O. Creutzfeldt,     Max-Planck-Institute of Biophysical Chemistry, Department of Neurology, D-3400 Göttingen, FRG

Publisher Summary

The cerebral neocortex is often considered as a screen on which the simple and complex functions of the organism are laid out like on a map and from where they need only to be retrieved by a highest order neuronal system, a specified area, or an agent. It has caught the interest of neurologists since the first proposal of Gall that psychological and characterological properties of the personality are represented in its different areas. This chapter discusses the functional specificity of a cortical area and the problem as to how the various functions are recombined into unity by considering the output connections of the cerebral cortex. The neocortex receives an orderly afferent input from the thalamus, and each area of the cortex has its specific thalamic projection nucleus. The primary thalamic input from the thalamus to the cortex is excitatory and also in this respect, the cortical areas do not seem to differ from each other.

The cerebral neocortex is often considered as a screen on which simple and complex functions of the organism are layed out like on a map, and from where they need only to be retrieved by a highest order neuronal system, a specified area or an agent. It has caught the interest of neurologists since the first proposal of Gall that psychological and characterological properties of the personality are represented in its different areas. But in spite of our ample knowledge on this part of the brain today, we are still far from a real understanding. The cortex has been endowed with the highest functions of the brain and, like no other part of the brain, the description and the often vivid arguments of the localization of such functions often reflect the philosophical backgrounds and the self-understanding of the authors rather than define these functions in terms appropriate to the brain /Creutzfeldt, 1975/. Human made models of personality, behavior, perception and intellect, from the idealistic psychology at Gall’s time, through the positivistic psychophysicism, association psychology at the turn of the century, the holistic Ganzheits-psychology of the early 20th century, to behaviorism, intellectualism and the modern computer-oriented age have left their terminology, and at the same their unsolved problems. I want to address, some aspects of the cortex which are general to the whole neocortex, then turn to what establishes the functional specificity of any cortical area and finally consider the problem of how the various functions are recombined into unity by considering the output connections of the cerebral cortex.

A Thalamo-cortical representation.

The neocortex receives an orderly afferent input from the thalamus, and each area of the cortex has its specific thalamic projection nucleus /Macchi, and Rinvik, 1976/. Although some or even most neocortical areas may receive an input from more than one thalamic subdivision or nucleus, and therefore thalamic nuclei may send inputs to more than one area, it becomes more and more clear that in the general layout and as a general principle, the neighbourhood relationship in the thalamus is preserved also in the projection to the cortex. As examples, the projections from anterior thalamic nuclei to the precentral and premotor cortex /Kievit and Kuypers, 1977/, from the medial geniculate and the posterior nuclei to the auditory cortex /Diamond, 1979/ and from the lateral geniculate and posterior nuclei to the visual cortex /Creutzfeldt, 1979, Shoumura, Watanabe and Creutzfeldt, 1981/ may be taken as examples.

We may generalize from these as well as from many other observations a topological representation of the thalamus on the neocortex. From this point of view, there is no neocortical area closer or further from the thalamus, and one might consider the thalamo-cortical relations as continuous with no need for subdivisions into nuclei and cytoarchitectonic areas. In fact, such is the situation in early development as it was remarked already by von Economo /1927/. Only later in development, morphological differentiation of both structures becomes evident, and in the mature brain such cytoarchitectural differentiations of cortical areas may coincide amazingly well with the nuclear subdivisions of the respective thalamic projection nuclei, as it is well demonstrated in various recent reviews /Creutzfeldt, 1979, Diamond, 1979, Macchi and Rinvik 1976, Sanides